Studies of breeding Sandwich Alistair J. M. Smith Photographs by Jan van de Kam Plates 16-23 INTRODUCTION It is opportune that a series of Jan van de Kam's wonderful photo• graphs of Sandwich Terns Sterna sandvicensis at a Dutch breeding colony (plates 16-23) should appear at a time when the European population is threatened at both ends of its range. The effects of human disturbance and ground predators in Scottish colonies and of trapping for food in West Africa have been highlighted recently (Bourne and Smith 1974). The disastrous effects of pollution at Dutch colonies in the 1960's are well known (Rooth and Jonkers 1972) and, although these colonies have shown signs of recovery, only about 3,500 pairs bred in 1973 (B. Speek verbally). Apparently half of the west European population now breeds in Britain and Ireland, where there are possibly 12,000 pairs (Cramp et al. 1974). The Sandwich is usually placed in the Sterna, but Moynihan (1959) related it to the crested 'Tkalasseus' terns and certainly its breeding behaviour seems more akin to that of such as the S. maxima (Buckley and Buckley 1972) and Caspian Tern Hydroprogne caspia (Bergman 1953) than to that of the smaller Sterna terns.

ARRIVAL AT BREEDING COLONIES The has a vast wintering range, extending from the north Mediterranean along the north and west coasts of Africa to the Cape and thence north-east as far as Mozambique (Miiller 1959, Langham 1971, C. J. Mead in litt.). Most breeding adults (three years and older) and some first- and second-year begin to return north from February. Adults assume breeding plumage from early February and I have seen aerial courtship from mid-February in Ghana. Once, in Sierra Leone, I encountered ground courtship as early as 20th January, while the birds were still in winter plumage. The first arrivals normally reach the south coast of England in March and it is not uncommon to find them at a breeding colony in northern Scotland at the end of March or early April. There is very little information on their behaviour at this time, but at Sands of Forvie, Grampian, their habit of visiting the colony immediately on arrival has given me an opportunity to study this

142 {Brit, Birds, 68: 142-156, April 1975} Sandwich Tern studies 143 stage. At first they tend to leave at dawn to fish along adjacent coasts, sometimes up to i£ km offshore. During the forenoon single birds, pairs or small groups only occasionally visit the colony, flying low over it and often alighting to preen or roost on the sandy foreshore. Visits increase around midday and then follows a period of and roosting. During the afternoon the terns gradually disappear, and they come in to roost only as darkness falls. It has been suggested that at this stage they spend most of the day fishing because of the scarcity of food in the surface layers of inshore waters, but this diurnal pattern is very similar to that which I have seen in West Africa during the two months prior to their departure north. Before mid-April there are terns at the colony throughout the day, but with a small peak in numbers around midday and early afternoon and a big influx at dusk. The Sandwich Tern's habit of nesting with more belligerent species, such as Black-headed ridibundus, is well docu• mented. Many years' study have shown that in northern Scotland it prefers to nest in early May, when its breeding success is likely to be enhanced. Perhaps for this reason, it tends to synchronise more readily with an early nester such as the Black-headed , which is on the colony from early March and lays in mid-April, than with the smaller terns which do not begin laying until mid- May. The influence of nesting Black-headed Gulls on Sandwich Terns in search of breeding sites has been discussed by a number of writers, such as Salomonsen (1947), Van den Assem (1954) and Isenmann (1972). At Forvie, from mid-April until laying time, the Sandwich Tern flock has in recent years moved at dusk into the Black-headed Gull colony until it is protected on all sides. This may be primarily for protection from ground predators, but it is possible also that the terns use the situation to gauge the suitability of the area for breed• ing. Although there are disadvantages in this association, Lind (1963) considered that the advantages were greater. The terns certainly benefit from the greater vigilance and aggressiveness of the gulls, but Rooth (1958) thought that the latter 'may be harmful to the tern populations on account of space competition, food parasitism, predation of eggs and predation of young birds'. In the Camargue, France, no predation of eggs and young was recorded in a mixed colony of Sandwich Terns and Black-headed Gulls (Isenmann 1972). Although gull predation of eggs and young occurs at Sands of Forvie, it does not seriously affect breeding success (though see pages 150-151).

COURTSHIP Colour-ringing at Forvie has shown that among the early arrivals 144 Sandwich Tern studies there are paired birds, some of which have been identified in pre• vious years. One pair nested in four successive seasons and, once paired, usually in the third or fourth year, the Sandwich Tern may well pair for life. Many other early arrivals are unattached or have poorly developed pair bonds, while later arrivals are almost always paired, though in mid-June there is an influx of unpaired two- and three-year-old birds (see pages 152-153). At first courtship is latent, especially in the earliest arrivals, but it requires only the appearance of a newcomer or a blink of sunshine to set off ground or aerial courtship. At this stage, however, particularly in the overcast weather of northern Scotland, it often quickly wanes. Prolonged sunshine encourages a continuation of courtship, especially aerial courtship. The typical 'high flight' (see below) has been described in considerable detail by Van den Assem (1954) and Cullen (1960a). It may be started by two or three (occasionally four or five) birds which have just flown in from the sea and arrived over the colony, or by members of the flock on the shore near the colony, or by a male in advertisement flight over the flock. The collective 'upflight' (Lind 1963), or rising up of the whole flock, is also often seen at this stage, precipitated by, for example, a movement of the tide, a corvid flying near, or the approach of a human being. Lind suggested that such com• munal flights may well influence the frequency of sexual behaviour, and certainly many high flights originate from them. The earliest high flight I saw in Ghana was triggered by an upflight when a Black Kite Milvus migrans flew over the flock roosting at a lagoon. An unmated male Sandwich Tern attracts the attention of the females by flying around over the flock, carrying a fish and calling a characteristic 'koreet'. Occasionally no fish is carried and the call then sounds more like 'kireet' or 'kirrik'. This is the male's advertisement flight. Alternatively he may alight in or near the flock and approach several birds, calling and raising his head and bill. Usually the wings are held away from the body and the crest raised in excitement. When he has the attention of a female, which may be when she also adopts the courtship display (plate 17), he takes off in an aerial 'bent posture', with head and bill pointed downwards and back slightly arched, and she follows him into the high flight. Other birds may join them. Circling, they climb rapidly until sometimes they are almost invisible even with powerful binoculars. Before they reach this height, the original male may be left with his female, but occasionally in the initial stages three, four or even five birds may stay together throughout and break up only after the fast downward 'glide' which often follows several false starts. The high flight may persist for some time, individual birds participating for up to ten minutes or longer before going Sandwich Tern studies 145 into a glide. In the glide the birds may fly very close, and on several occasions I have seen them touch at the 'pass' when one overtakes another, which happens a number of times during the descent. The overtaken goes into the bent posture described above, while the other, if paired to it, appears normal (Cullen 1960a); but where a number of birds are participating I have seen both go into the bent posture at the pass. The overtaken bird, especially if carrying a fish, may also raise its wings over its back, sometimes beating them slightly; this has been termed 'V-flying', which describes the action well. The calls during the high flight are characteristic. During the upward part both birds give 'koreet', 'kek', and 'arrie' or 'erre' calls (Van den Assem 1954), and R. Chestney (verbally) thinks that the sexes can thus be differentiated, the female calling noticeably higher than the male. During the glide a quickly repeated 'kekekekekekekek' is uttered by both birds, especially the bent one at the pass. Following the glide, and depending on the development of the pair bond, the participants may break off to fish, preen, or go into ground courtship or often into another display flight described very well by Van den Assem (1954): 'The flight occurs in a particu• lar way: the wings are thrust emphatically through the beat, by which the body without actually advancing more quickly gets a push upwards so that the flight looks like a dance'. Overtaking also occurs in this display, and before being overtaken the leading bird opens its bill wide, with head lifted slightly, and calls a nasal 'wah' suggesting to me a loud yawn. This call is also given commonly on the ground, with head and neck held in the same attitude, not only during courtship but also from birds making nest reliefs (page 150); it has been described as an ambivalent call indicating strong escape tendencies (Van Iersel and Bol 1958). As the birds become used to one another it is heard less often in this context. It is also heard in the colony as an alarm: aggressive terns have flown out from the colony to meet me with this peculiar dancing flight and 'wah' call before changing to normal flight and scolding me with a harsh 'kekekek'. In ground courtship there are a number of variations and inten• sities of stretch posture. One has been termed the 'pole stance' (Van den Assem 1954) and is equivalent to what was termed the 'erect, posture' by Dr J. M. Cullen (in Bannerman 1962); stretch postures are illustrated in plate 17 and the pole stance (or erect posture) in plate 19a. Van den Assem and P. M. Schenk (in Van Iersel and Bol 1958) considered that 'the ambivalent (aggression- escape) stretch posture consists of more or less independently varying elements such as neck stretching, ruffling or depressing the crest 146 Sandwich Tern studies and neck feathers, lifting the wings. Depending on the relative strengths of these elements, the stretch posture indicates a greater or lesser predominance of the escape drive'. The pole stance is often adopted after a high flight and, since this appears to be the strongest indication of the escape drive, it may serve in this context to decrease the aggression latent in the high flight which contains overtly hostile elements (Cullen 1960a). Dr Cullen (in Bannerman 1962) suggested that the Sandwich Tern probably also had the 'ground bent posture' of the S. hirundo (like the male in plate 17b, but with neck vertical and stretched higher, and head and bill angled downwards). Van Iersel and Bol did not agree, but in my experience males do adopt a posture with some elements analogous to it. If a female approximates this position in courtship with a male, she rarely allows her bill to be angled below his. Typical of three birds coming in from the glide to alight on the shore was the following. The leading one, a female, landed and immediately went into the pole stance with wing 'arms' spread wide and wing tips below the tail on the sand (plate 19a). The second bird, a male carrying a fish, alighted and held the fish in his bill as in Cullen's ground bent posture. The female lowered the intensity of the stretch to a moderate stretch posture, with bill slightly raised, and walked around the male (plate 17b). She then went into the begging position (plate 18a) and immediately the male jumped on her back, holding the fish. This attempted copula• tion was interrupted by a second male which had circled above, making a low pass in the bent posture. The female then flew off in the bent posture, dislodging the male which followed her similarly. Copulation commonly occurs on the shore between pairs on their own or in a flock. It may precede scraping, but often there have been visits to the subcolonies where the male leads in a posture approaching the ground bent, with the female in a moderate stretch posture. When they have selected a suitable spot, which may coincide exactly with the one used in previous years, both birds examine it with bills down and may scrape, though initially only the male does so. During these ceremonies it is not unusual for both to adopt the pole stance with much head turning, and then gradually assume the stretch posture as before. As copulation approaches, the soliciting female utters a 'quee-quee-quee' call in a begging posture similar to that of a chick about to be fed (compare the female in plate 18a with the chick in plate 22b). She may attract a male from the air using this call, but it is a particular male and not a chance contact. The male, normally in her company for some time, usually goes into a moderate stretch position with horizontal or lowered bill, and calls a deep-throated 'kuk-kuk'. He tries to circle, pre• sumably to get into a position to mount, but she keeps facing him Sandwich Tern studies 147 and calling a persistent 'quee-quee-quee' (plate 18a). Eventually he jumps on her back and finally lowers his legs and waggles his tail as he bends himself under her until the cloacae make contact (plate 18b). I have counted up to eight contacts in one mounting and more are apparently not uncommon (Van den Assem 1954). Sometimes the female unmounts her partner by walking from beneath him, or a copulation is disturbed by other birds. When this happens the male may press his cloaca on the sand, waggling his tail to and fro as during copulation, and may ejaculate. The pole stance may be adopted immediately after copulation when it may be broken off quickly as the partners go into a bout of preening, or preening may begin immediately. As in the Royal Tern (Buckley and Buckley 1972), incubating females may be mounted, but I have not seen this happen to a brooding female.

COLONY STRUCTURE The physical layout of a colony may be simple or complex. Dircksen (1932) found a single large colony in some years and a number of separate ones in others, for no apparent reason. The change did not appear to increase breeding success, as it often encouraged predation by Herring Gulls L. argentatus. On the Fames and Coquet Island, Northumberland, where the development of a single large colony is possible, this occurs only at the former. Dr N. P. E. Langham (in lift.) suggests that the dense nesting habit of this species has necessitated the division into subcolonies as an adaptation against ground predation; synchronised breeding in a particular subcolony has arisen by pairs in the same physiological condition being attracted to other pairs that have already settled in a nesting place. While this is certainly true, at Sands of Forvie grouping may begin long before the terns have settled in their nesting areas: subcolony populations of colour-ringed birds have been watched sorting themselves out on the shore, and these same groups later occupy the various subcolony areas. Originally at Forvie, the birds nested rather loosely in one colony with a rather long breeding time. As this grew in size the nature of the sand dunes precluded its development, and subcolonies grew up, each having a shorter breeding time than the colony as a whole. It is common for the early, more highly synchronised, subcolonies to have young flying before the late ones have hatched their eggs. At Scolt Head, Norfolk, terns breed on embryo dunes which allow the formation of a single large colony or a number of subcolonies. From his experience there, Chestney (1970) suggested that adverse weather is responsible for the formation of subcolonies: for example, a single large colony was formed during fine weather in 1965 but the following year, during periods of adverse weather, seven sub- 148 Sandwich Tern studies colonies were formed. Bad weather does affect the start of laying at subcolonies, but other factors, including human disturbance, ground and aerial predators, may also be responsible. Langham (1974) suggested that the subcolonial habit becomes superfluous at safe, long-established sites like the Fames where groups tend to merge into one another, and presumably, in the absence of ground predators, one might expect a single large colony to develop even• tually on Coquet Island.

LAYING AND INCUBATION The eggs are laid at any time of the day or night, apparently mosfly between 18.00 and 06.00. In 1974 at Sands of Forvie the first egg was laid just after midday, and its owner incubated it alone in the middle of a group of Black-headed Gulls while the other Sandwich Terns in the subcolony, which had been scraping and courting, left to roost on the shore in the early afternoon, returning later. The nest is commonly nothing more than a scrape in sand or a slight depression in or on vegetation. Occasionally a Sandwich Tern appropriates a Black-headed Gull's nest vacated when a particularly dense group of terns starts to nest among the gulls. Most gulls persist, however, and the terns group themselves around or between their nests. After incubation begins, many nests become quite substantial due to the billing of straws and other material into the hollow by the sitting bird (plate 19b). This behaviour is an extension of the formalised straw-tossing in which Sandwich Terns engage, in common with other terns and gulls (Tinbergen 1935, Palmer 1941). Relieved birds often pick up material, even grains of sand, as they leave the nest, and drop or toss it sideways and to the rear. Clutches are normally of one or two eggs. Less than 1 % are of three, some, though not all, clearly resulting from rolled eggs or two females laying in one nest (see below). Over half the pairs may have one-egg clutches in one season, with the reverse the following year. Clutch size also varies during a season, in general being higher at peak laying periods in subcolonies and higher in early subcolonies than in later ones (see also Langham 1974). Occasionally in two-egg clutches the egg colorations are clearly different and one suspects that two females were involved. Colour-ringing has shown that it is not uncommon for two females to lay in one nest, particularly among three-year-old birds breeding for the first time, though it has also been recorded in one bird seven years old. I have recorded multiple relationships in which two males and one female were on one egg, one male and two females on two eggs, and (once) two males and two females at one nest containing two eggs. There were key birds in each case, and no nest relief took place unless the Sandwich Tern studies 149 key bird was either relieving or being relieved. None of these relation• ships persisted to the hatching time. The laying interval in two-egg clutches varies from two to five days, and incubation averages about 25 days and may extend from 21 to 29 days. Dr N. P. E. Langham {in litt.) found that the first Sandwich Terns to lay on Coquet appeared to leave the island at night and return in the morning to their eggs, but I have found no evidence of this at Sands of Forvie. It may be connected with their familiarity with the site: in 1965 on Coquet the terns began laying only two days after arrival, and in 1966 four days after, whereas Sands of Forvie birds are much more familiar with the colony, many having been in the vicinity for up to a month and having roosted in the colony area for up to two weeks before laying. The synchronisation of arrival and laying is thought to be an important anti-predator device (Cullen 1960b): intervals of three or four days in the Camargue (Isenmann 1972) and of five at Scolt Head (Chestney 1970), as well as Langham's two to four days, confirm that this synchronisation exists. My own experience is clearly different, and it is interesting that at Langenwerder, East Germany, Nehls (1969) reported that in 1968 the Sandwich Terns occupied the colony from 4th April but it was not until 25th April that the first egg was found. It is difficult to account for this widely divergent behaviour. There is a direct correlation between breeding synchronisation and nest density. In a highly synchronised subcolony the inter-nest distance is the bare minimum for successful breeding. Some birds occasionally lay too close to their neighbours, which causes pro• tracted bickering and probably the desertion or failure of one or more of the clutches so affected (see also Dircksen 1932, Ansingh et al. i960). In such dense colonies the question of nest and egg recognition arises. It has been stated that egg colour variation assists adult Royal Terns in locating their eggs among the many thousands in a typical colony, though some aspects of nest location also have a significant effect (Buckley and Buckley 1972). I have trapped large numbers of Sandwich Terns on the nest and substituted plaster- filled blown eggs during the critical period before the clutch was covered by the other bird of the pair. In no case were these eggs rejected, though often quite different from the real ones, and no problems were experienced on the return of the original eggs at a later date. It seems clear that skill in egg recognition as well as nest location is essential in the relatively featureless Royal Tern colonies with their thousands of clutches, but a highly developed skill in nest location is probably sufficient for Sandwich Terns at a colony such as Forvie where characteristic features of topography are plentiful. 15° Sandwich Tern studies Within dense subcolonies, it is obviously impossible for copulation, preening and so on to take place, and indeed it is often difficult for birds to make nest reliefs. Both sexes have brood patches and share in incubation. Reliefs are usually accompanied by courtship displays, as previously described, which tend to diminish in intensity as incubation progresses; before the halfway stage some take place without noticeable display. The male feeds his mate regularly at first, but the frequency of feeding may also decrease as incubation progresses. It is not unknown for an incubating female to rise from the nest, fly off to fish and return to incubate a few minutes later. Reliefs occur at regular intervals between birds of a pair, but there are wide variations between pairs. Some females are loath to move off eggs, particularly if the male is a good provider, and when they do it is only for a short time. On their return they quickly try to relieve the male and, if he is unwilling to move, may physically push him off the nest. Other pairs seem content to share incubation equally, but some change at intervals as short as 15 minutes or as long as nine hours overnight. I have never seen a nest relief during the hours of darkness (23.00 to 02.30 BST). In dense subcolonies there is much threat behaviour between incubating birds, called gackering. This 'consists of turning the bill and stretching the neck—of which the plumage is more or less ruffled —towards the opponent, and uttering a hoarse rhythmic "gagaga" or "gegege" ' (Van Iersel and Bol 1958). The bill is characteristically held fairly wide open, though in the least intense form the bill is turned and the neck stretched without further movement or calling. (A variant of the gackering call, resembling a fat quacking, is uttered by fishing terns which come too close to one another, and I have heard it, probably as a warning signal, from birds fishing in fog.) Gackering can develop into pecking or grasping of bills if the other bird,reacts aggressively, but sometimes it does not respond. It is also directed at aerial predators such as Black-headed Gulls (plate 20), which fly too low when either searching for uncovered eggs or intent on taking fish from incoming terns. During such attacks the gackering calls can become quite intense, and in my experience usually deter these gulls from uncovered eggs but hardly do so at all when they are pursuing terns flying in-with fish to feed chicks. Gackering rarely deters Herring Gulls; Dr E. Fuchs {verbally) has even seen one boldly push a gackering tern off its nest on the perimeter of a subcolony and take its egg. In 1972 at Forvie, in a particularly dense subcolony of 400 pairs surrounded by Black-headed Gulls' nests, almost half of the second chicks starved because of intense kleptoparasitism by the gulls. This was the first evidence in 16 years' study that such parasitism seriously affected the terns' breeding success. None of the remaining Sandwich Tern studies 151 1,600 pairs in several subcolonies was affected in this way during that season. The Sandwich Tern's habit of advertising the colony by a radial whitewashing of droppings around the nest has been described many times. The eggs are said to match the guano-spattered back• ground (Cullen 1960b), but on a dense mat of green vegetation in a typical island habitat such as on Coquet or the Fames, this white• washing appears, to the human eye at least, to draw attention to the eggs. On sand, however, it seems to provide better camouflage (Chestney 1970).

POST-HATCHING BEHAVIOUR When the eggs hatch, the shells are usually billed out of the scrape by one of the adults but are left to litter the colony, blowing to and fro in the wind. There seems, therefore, little effort to camouflage the colony; presumably synchronised breeding in dense colonies confers advantages which make such anti-predator devices no longer necessary (Cullen 1960b). Disturbance at hatching induces a speedy movement of the chicks away and I have often found second eggs left in the nest scrapes (see also Chestney 1970). Most writers agree that the exodus occurs from the third day, but in 1970 at Scolt Head Chestney showed me young fledging where they had hatched because the colony was completely undisturbed that season. I have also noticed that chicks left within three days of hatching at sub- colonies used for research and visited daily, while at others in the same colony, which were undisturbed, the exodus was much slower. The chicks are led away by their parents using an encouraging call similar to the male's when he leads a female to scrape: a 'koreet' with head and bill raised at each call (plate 21b). The behaviour of adults and chicks thereafter seems to differ in certain respects from colony to colony. The so-called creche behaviour appears to be facultative in western . At Sands of Forvie the chicks disperse throughout the colony area of marram sand dunes and never stray far from cover. When danger approaches they hide in the vegetation or occasionally crouch on open sand or pebbles. Some scrape 'funk-holes' in the sand, usually under cover, and are found there on every visit to the colony, though others move about the entire area and are never found in the same place twice. Normally two-chick families stay together, but I have found siblings in widely separated parts of the colony for most of the fledging period—28-30 days—so they were presumably fed by different parents. (These observations were made before I discovered three- bird relationships, and it is possible that two females were involved.) 152 Sandwich Tern studies I have records of marked siblings being fed only by the female. The classic creche of Sandwich Tern type was well described for the Royal Tern by the Buckleys (1972): '. . . a creche may be loose and strung out over a wide area at the colony site (a relaxed creche), or it may become a tightly packed mass of moving chicks (an alarmed creche). . . . The degree of spread of the relaxed creche is a function of cover, island size, nearness to water and size of area accommodating the creche. At an alarm,... the chicks coalesce into one or more very tight masses, moving, amoeboid, as a unit away from the disturbance'. In 16 years at Forvie, this has happened, to my knowledge, on only four occasions, during considerable human disturbance. Only a small proportion of the available chicks took part, most remaining in hiding, and the colony returned to normal very soon after the removal of the disturbance. Marples and Marples (1934) gave a good account and included a photograph of a classic creche at Blakeney Point, Norfolk, though I have never seen one at nearby Scolt Head. On the Fames the chicks almost always 'troop' (the local term for an alarmed creche), though on Coquet I found that alarmed chicks preferred to crouch in cover rather than form a creche. There is a great deal of inter• change between the Fames and Forvie birds, yet the behaviour at each colony does not appear to be affected. Where creching occurs, it is interesting to watch adults returning from a fishing expedition to look for their young, often among many hundreds of birds. It is easy to understand the former belief (see Armstrong 1947) that young in creches were fed indiscriminately by any fish-carrying adult. Long before this, however, Steinbacher (1931) was of the opinion that chicks were fed only by their own parents. During 1960-63 I colour-ringed a large sample of adults and their chicks, and subsequent observation on the shore flock, comprising fledglings and young about to fledge, showed no excep• tion to Steinbacher's belief. Often two- and three-year-old birds, and occasionally four-year-olds, possibly all non-breeding, attempted to feed young at random, but all their offers were rejected. I have several records of such young making an aggressive response like gackering, but lacking the adult's characteristic calls, towards these 'intruders'. I suspect that during a lean period the young would steal any such offerings; in Royal Tern creches alien chicks occasion• ally grab food from an adult before it can feed its own chick (Buckley and Buckley 1972). Normally during early June the number of three-year-old birds in the colony increases. Some breed but it is unusual for many of the late arrivals to do so. With a few two-year-olds which arrive in mid-June, some four-year-olds and a few older birds, these are the non-breeders whose numbers fluctuate from year to year. Sandwich Tern studies r53 They spend a lot of time courting and scraping in the subcolonies, and when chicks appear often carry fish and attempt to feed any that happen to incite the feeding urge. As previously mentioned, they continue this behaviour in the shore flocks of fledglings.

POST-FLEDGING BEHAVIOUR Post-fledging dispersal begins in late June or early July, often as soon as the young fledge. I have observed Forvie juveniles in the Moray Firth and up to 65 km south of the colony only three days after fledging. The urge to disperse so quickly may be motivated by the high density at the breeding colony as the result of syn• chronous hatching of large numbers of young (see also Isenmann i972)-_ During this dispersal the young terns continue to be fed by their parents, though often by only one, probably the female. Feeding occurs on land or water and, when conditions permit, there seems to be a preference for feeding on the surface of the sea or on an estuary, but occasionally on flotsam or salmon-fishing nets and poles. The juvenile, calling querulously 'chee-chee-chee', alights on the surface for a moment and the adult may pass the food over without alighting. On land the attitude adopted by the young bird (plates 22b, 23) and its begging call are reminiscent of the pre-copulatory display and call of the adult female (page 146). Juveniles imitate the hunting technique of their parents, quartering the sea or estuary and hovering, but at a much lower average height. They practise dipping at small sticks, seaweed or other flotsam which they pick up and drop again and again. Plunge-diving appears to bring little or no success at first, though within a few weeks success is achieved, particularly with stranded fry in shallow pools. Langham (1971) found that dispersal was directed nearly equally north and south. On the .east coast of Britain there is certainly an annual movement of adults with young to traditional feeding grounds in the Moray Firth and elsewhere off eastern Scotland in July, August and September. Juveniles from the Fames and Forth appear off Forvie in July and August each year and often remain there until mid-September before returning south; for example, in 1974 the first Fames juveniles were at Forvie on 22nd July, mixing in the shore flock with the local birds. Breeding recommenced at Forvie after a prolonged lapse, and adults controlled there in the first few years originated in the Fames and Forth. Some adults and young remain in the colony area until at least late August (and perhaps mid-September), while others must migrate immediately or soon after they leave the colony, since there are ringing recoveries from Ghana at the beginning of September. 154 Sandwich Tern studies When the last birds pass south along the east coast in late September and sometimes October, the young are still dependent on parental care. The skills of the highly specialised feeding techniques are not learned quickly and little is known about the duration of parental dependence. In January and February 1970, in Sierra Leone and Ghana, it appeared to me that all dependence had ceased, though Dunn {1972), who was in Sierre Leone at the same time, saw one first-winter bird persistently following an adult throughout a fishing session, and it is possible that dependence may continue in some young birds. Indeed, in the Royal Tern feeding of the young has been seen in December and January in winter quarters in Peru (Ashmole and Tovar S 1968) and well into February and March on Bonaire Island, Lesser Antilles (Buckley and Buckley 1972). The calls of adults and young change towards the end of the year, and in January and early February 1970 the only call I heard in West Africa was a monosyllabic call rendered 'krik' by Dunn (1972), though I thought it was 'djeet'. I have since heard and recorded this call from a few adults and young fishing in late September and early October in this country. I heard the first characteristic 'kirrik' during aerial courtship in Ghana in mid- February, by which time adults have begun to resume breeding plumage and move north again.

ACKNOWLEDGEMENTS I should like to acknowledge the financial assistance received from the Nature Conservancy Council who also gave me permission to work at the Sands of Forvie National Nature Reserve, Grampian. My thanks are also due to the Frank Chapman Memorial Fund of the American Museum of Natural History and to the Royal Society for financial assistance in mounting an expedition with Dr N. P. E. Langham to West Africa in 1970.

SUMMARY Certain aspects of the behaviour and breeding biology of the Sandwich Tern Sterna sandvicensis are reviewed and described in general terms. The colony at the Sands of Forvie, Grampian, is contrasted with others on the east coast of Britain and in Europe. The terns were found at the breeding colony at Forvie from their arrival usually in early April until laying time a month later. Previous writers have postulated synchronised arrival and laying in the Sandwich Tern, but the Forvie and apparently Langenwerder, East Germany, colonies seem to be exceptional. At both sites terns are on the colony from three weeks to a month before the first eggs are laid. Courtship commenced immediately on arrival at the colony, and displays such as the male advertisement flight, the high flight and glide, the various stretch postures, scraping and mating are described. Sandwich Terns may nest in one large group or several small groups or sub- colonies within a colony. These adaptations are discussed and it is suggested that subcolony nesting may be an adaptation against ground predators, although other factors such as human disturbance and weather may contribute to this effect. Multiple relationships at one nest were proved by colour ringing, and some appear to account for differently coloured eggs in some two-egg and probably Sandwich Tern studies *55 three-egg clutches. The presence of key birds was essential for nest reliefs to take place. Mainly three-year-old birds were involved in these relationships and none was seen to persist until hatching time. Crecheing behaviour appears to be facultative in western Europe and occurs consistently in Britain only at the Fame Islands colonies. The influence of the Black-headed Gull LOTUS ridibundus on the breeding of the Sandwich Tern is reviewed and its effect on the breeding success of the terns is discussed. In only one season in 16 at Forvie was kleptoparasitism by the gulls on the terns shown to have a serious effect on chick mortality. Observation on colour-ringed adults and their chicks confirmed the belief that adults fed only their own chicks, although other adults, possibly non-breeders, attempted to feed chicks and fledglings at random. Post-fledging dispersal takes place from the time the young can fly at 28-30 days to traditional feeding areas and in some cases seems to merge quickly into migration, since ringing recoveries indicate arrival in West Africa in early September. Parental dependence in juveniles has been observed in Britain until the last birds pass south in October, but seemed to have ceased by January in West Africa. The characteristic calls of adults and juveniles were not heard in West Africa and only a call rendered 'djeet' was recorded. The first 'kirrik' was heard in mid-February in Ghana.

REFERENCES ANSINOH, F. H., KOELERS, H. J., VAN DER WERF, P. A., and Voous, K. H. i960. 'The breeding of the Cayenne or Yellow-billed Sandwich Tern in Curacao in 1958'. Ardea, 48: 51-65. ARMSTRONG, E. A. 1947. Bird Display and Behaviour. London. ASHMOLE, N. P., and TOVAR S, H. 1968. 'Prolonged parental care in Royal Terns and other birds'. Auk, 85: 90-100. BANNERMAN, D. A. 1962. The Birds of the British Isles. Edinburgh and London. vol. 11. BERGMAN, G. 1953. 'Verhalten und Biologie der Raubseeschwalbe (Hydroprogne tschegrava)'. Acta Zool. Fenn., 77: 1-50. BOURNE, W. R. P., and SMITH, A. J. M. 1974. 'Threats to Scottish Sandwich Terns'. Biol. Conserv., 6: 222-224. BUCKLEY, F. G., and BUCKLEY, P. A. 1972. 'The breeding ecology of Royal Terns Sterna () maxima maxima'. Ibis, 114: 344-359. CHESTNEY, R. 1970. 'Notes on the breeding habits of Common and Sandwich Terns on Scolt Head Island'. Trans. Norfolk Norwich Nat. Soc, 21: 353-363. CRAMP, S., BOURNE, W, R. P., and SAUNDERS, D. 1974. The Seabirds of Britain and Ireland. London. CWLLEN, J. M. 1960a. 'The aerial display of the and other species*. Ardea, 48: 1-37. 1960b. 'Some adaptations in the nesting behaviour of terns'. Proc. Int. Orn. Congr., 12: 153-157. DIRCKSEN, R. 1932. 'Die Biologie des Austernfischers, der Brandseeschwalbe und der Kustenseeschwalbe nach Beobachtungen und Untersuchungen auf Norderoog'. J. Orn., 80: 427-521. DUNN, E. K. 1972. 'Effect of age on the fishing ability of Sandwich Tems Sterna sandvkensis'. Ibis, 114: 360-366. ISENMANN, P. 1972. 'Sterne caugek en Camargue*. Nos Oiseaux, 31: 150-162. LANGHAM, N. P. E. 1971. 'Seasonal movements of British terns in the Atlantic Ocean'. Bird Study, 18: 155-175. ——— 1974. 'Comparative breeding biology of the Sandwich Tern'. Auk, 91: 255-277- 156 Sandwich Tern studies LIND, H. 1963. 'Nogle sociale reaktioner hos terner' (English summary: 'Notes on social behaviour of terns'). Dansk Orn. Form. Tidsskr., 57: 155-175- MARPJLES, G., and MARPLES, A. 1934. Sea Terns or Sea Swallows. London. MOYNIHAN, M. 1959. 'A revision of the family (Aves)'. Amer. Mus. Novit., no. 1928. MUIXER, H. 1959. 'Die Zugverhiiltnisse der europaischen Brandseeschwalben (Sterna saruhhensis) nach Beringungsergebnissen'. Vogelwarte, 20: 91-115. NEHLS, H. W. 1969. 'Zur Umsiedlung, Brutortstreue und Brutreife der Brandsee- schwalbe {Sterna sandvkensis) nach Ringfunden auf Langenwerder*. Vogelwarte, 25: 52-57- PALMER, R. S. 1941. 'A behavior study of the Common Tern (Sterna hirundo hirundo L.)'. Proc. Boston Soc. nat. Hist., 42: 1-119. ROOTH, J. 1958. 'Relations between Black-headed Gulls (Larus ridibundus) and terns (Sterna spec.) in the Netherlands'. Bull. Int. Comm. Bird Pres., 7: 117-119. ———, and JONKERS, D. A. 1972. 'The status of some piscivorous birds in the Netherlands'. TNO-nuuws, 27: 551-555. SALOMONSEN, F. 1947. 'Maagekolonierne paa Hirsholmene' (English summary: 'The gull-colonies on Hirsholmene'). Dansk Orn. Form. Tidsskr., 41: 174-186. STEINBACHER, G. 1931. 'Beitrage zur Brutbiologie von Silbermowe und Brandsee- schwalbe'. J. Orn., 79: 349-353. TINBERGEN, N. 1935. 'Field observations of East Greenland birds'. Ardea, 24: 1-42. VAN DEN ASSEM, J. 1954. 'Waarnemingen over het gedrag van de Grote Sterns'. Levende Mat., 57: 1-9. VAN IERSEL, J. J. A., and BOL, A. C. A. 1958. 'Preening of two tern species. A study on displacement activities'. Behaviour, 13: 1-87.

Supt Alistair J. M. Smith, Scottish Police College, Tulliallan Castle, Kincardine-on-Forth, Alloa, Central Region PLATE 16. Unmated male Sandwich Tern Sterna sandvicensis, Waddensee, Netherlands, attracting the attention of the fe• males by flying around over the flock carrying a fish, or by alighting in or near the flock and calling with persistent 'koreet' (pages 142-156) {photos: Jan van de Kam) PLATES 17-18. Fish-carrying male Sandwich Tern eliciting courtship display from female in moderate stretch posture with wing-arms held wide; this leads to aerial courtship in early stages of pairing and to scraping and copulation later. Below, a display which often follows if fish accepted and swallowed by female (male on left). Upper right, pre-copulatory behaviour in which female (right) adopts begging posture and calls persistently 'quee-quee-quee', and male posi• tions himself for mounting. Lower right, numerous cloacal contacts may occur at one mounting; female may unmount partner by walking from beneath him, or copulation may be disturbed by other birds (pages 145-147) {photos: Jan van de Kam) *. NM£* «■*

S£^ " A

1 PLATE 19. Above, 'pole stance' or 'erect posture'—most intense form of stretch posture—commonly seen immediately after two birds land from the 'high flight', during scraping and after copulation (pages 144-147). Below, empty shells are billed out of scrapes but left to litter colony (page 151) (photos: Jan van de Karri) PLATE 20. Black-headed Gull Larus ridibundus moving in to steal fish from in• coming Sandwich Tern. The majority of sitting birds are 'gackering' intensely, and the noise and threat produced would usually keep egg-stealing gulls away but rarely deter those bent on stealing fish (page 150) {photos: Jan van de Kam) PLATE 21. After hatching, nest reliefs continue and both sexes feed the young (head moult, on left, may affect 10% of breeding birds by first week of June). Below, from the third day the chicks arc led away by their parents; adult in centre is 'gackcring' mildly at the flying bird (page 151) (photos: Jan van de Karri) PLATE 22. Above, well-grown young Sandwich Tern exercising its wings, remain• ing fairly close to cover; fledging period is normally 28-30 days. Below, well- feathered chick adopting normal food-begging posture and calling a querulous 'chee-chee-chee' as adult flies in with fish (page 153) {photos: Jan van de Karri) PLATE 23. Adult Sandwich Tern feeding juvenile, illustrating an exaggerated form of the food-begging posture that is often adopted when adults have to make a very fast delivery to avoid fish predators, such as gulls and skuas (photo: Jan van de Kam)